Parasites of Amphibians and Reptiles from Michigan: A Review of the Literature

Transcription

1 STATE OF MICHIGAN DEPARTMENT OF NATURAL RESOURCES Number 2077 January 2005 Parasites of Amphibians and Reptiles from Michigan: A Review of the Literature Patrick M. Muzzall FISHERIES DIVISION RESEARCH REPORT

2 MICHIGAN DEPARTMENT OF NATURAL RESOURCES FISHERIES DIVISION Fisheries Research Report 2077 January 2005 Parasites of Amphibians and Reptiles from Michigan: A Review of the Literature Patrick M. Muzzall The Michigan Department of Natural Resources (MDNR), provides equal opportunities for employment and access to Michigan s natural resources. Both State and Federal laws prohibit discrimination on the basis of race, color, national origin, religion, disability, age, sex, height, weight or marital status under the Civil Rights Acts of 1964, as amended, (1976 MI P.A. 453 and 1976 MI P.A. 220, Title V of the Rehabilitation Act of 1973, as amended, and the Americans with Disabilities Act). If you believe that you have been discriminated against in any program, activity or facility, or if you desire additional information, please write the MDNR Office of Legal Services, P.O. Box 30028, Lansing, MI 48909; or the Michigan Department of Civil Rights, State of Michigan, Plaza Building, th Ave., Detroit, MI or the Office of Human Resources, U. S. Fish and Wildlife Service, Office for Diversity and Civil Rights Programs, 4040 North Fairfax Drive, Arlington, VA For information or assistance on this publication, contact the Michigan Department of Natural Resources, Fisheries Division, Box 30446, Lansing, MI 48909, or call This publication is available in alternative formats. Printed under authority of Michigan Department of Natural Resources Total number of copies printed 160 Total cost $ Cost per copy $3.13

3 Suggested Citation Format Muzzall, P. M Parasites of amphibians and reptiles from Michigan: A review of the literature Michigan Department of Natural Resources, Fisheries Research Report 2077, Ann Arbor.

4 Michigan Department of Natural Resources Fisheries Research Report 2077 Parasites of Amphibians and Reptiles from Michigan: A Review of the Literature Patrick M. Muzzall Michigan State University Department of Zoology Natural Science Building East Lansing, Michigan Abstract. A summary of the literature on the parasites (protozoans, digenetic trematodes, monogeneans, cestodes, and nematodes) of amphibians and reptiles (herps) in Michigan is presented. It is divided into three sections: 1.) a list of the parasite species by taxonomic group and family followed by their herp hosts and studies, 2.) a list of the herp species in Michigan by order and family and their parasites, and 3.) a list of body sites occupied by parasites in herps by order. At least 84 studies (abstracts and articles) have been published on the parasites of herps in Michigan from 1916 through These studies include: 49 on frogs, 5 on toads, 19 on salamanders, 15 on snakes, and 16 on turtles. The more widespread or common herp species have more parasite species reported from them compared to the less common species. At least 17 protozoan species, 39 adult digenetic trematode species, 12 larval digenetic trematode species, 2 adult monogenean species, 5 adult cestode species, 2 larval cestode species, 15 adult nematode species, and 3 larval nematode species have been reported from herps in Michigan. Acanthocephalans have not been reported in Michigan herps. Only two studies have been published on the parasites of herps in the Upper Peninsula of Michigan. Nineteen (36%) of the 53 herp species in Michigan have not had articles published on their parasites. This study is the first one to summarize the parasites of herps in a state or province in North America. The literature on the parasites of herps (defined here as amphibians, snakes, turtles, and lizards) in the central United States is extensive, diverse, and scattered. Historically, studies have focused on two major areas, parasite life histories and taxonomy. Parasite fauna surveys have also received considerable attention. However, many of these surveys are limited in that only one parasite species or parasite group was studied, only one herp species was studied, or the number of herps examined was small. More studies have been performed on the parasites of amphibians than reptiles. Dyer (1991) listed many of the helminth parasites of amphibians from Illinois and adjacent midwestern states. Andrews et al. (1992) provided a checklist of helminths in bullfrogs Rana catesbeiana in North America. Prudhoe and Bray (1982) discussed the helminth parasites of amphibians. Ernst and Ernst (1977) listed the helminths infecting native turtles of the United States. Baker (1987) provided a synopsis of the nematodes parasitic in herps of the world. Kuzmin et al. (2003) reviewed and summarized the literature on the nematode genus Rhabdias from herps of the Neartic. Aho (1990) presented and explored mechanisms influencing the patterns and processes of helminth community organization in herps. Based on discussions with parasitologists and herpetologists as well as reviewing articles on the parasites of herps, it became apparent that 1

5 many investigators were unaware of the existence of published information on the parasites of Michigan herps. This might be because titles of some articles do not indicate that parasites of Michigan herps were studied. Furthermore, the information in some older articles is difficult to interpret, often not indicating specifically what species of herps were examined, where in Michigan the study was performed, and if the study was actually done in Michigan. The objective of the present study was to summarize information on the parasites of herps in Michigan in an accessible form, as the literature on this subject is widely scattered in several journals. For investigators interested in these parasites and herp groups, this review will provide a basis for a better understanding of this subject and for future study. Infectious diseases, such as chytridiomycosis, ranavirus, saprolegniosis, and trematode (Ribeiroia sp.) infection have been discussed as causes of mortality leading to amphibian population declines (Daszak et al. 2003). Another objective of this study, therefore, was to determine if relationships between helminths and amphibian mortalities and malformations have ever been reported in Michigan. Furthermore, it is important to document parasites of herps in Michigan so that changes brought about by environmental variation and the introduction of exotic organisms can be understood. Methods Ten species of salamanders, 13 species of frogs and toads, 18 species of snakes, 10 species of turtles, and 2 species of lizards occur in Michigan (Harding and Holman 1990; Harding and Holman 1992; Holman et al. 1989; Harding 1997). Information on the parasites of herps in Michigan was obtained from studies published since 1916, when the first study was published. Some studies report experimental infections of herps with parasites. Several studies occurred in the Douglas Lake and Ann Arbor areas, and have been designated to occur in Cheboygan County and Washtenaw County, respectively. In most situations, no attempt has been made to demonstrate the past complexities of parasite synonyms or to review the validity of published results. Studies on viruses, bacteria, fungi, and leech parasitism of herps from Michigan were not included. Results The parasites found in herps of Michigan, by taxonomic group and family, are listed in Table 1. The numbers of parasite species counted, presented, and reported in the text only involve those identified to species, unless only one genus or common name was reported in the original article. A total of 17 protozoan species (1 ameba, 10 flagellates, 2 ciliates, 4 apicomplexans) in 9 families have been reported in herps. Six studies involved some aspect of Cepedietta michiganensis infecting the four-toed salamander Hemidactylium scutatum. Only Entamoeba invadens, Trichomonas sp., coccidians, and a haemogregarine-like form have been reported from snakes. Only one protozoan Haemoproteus metchinikovi has been reported from a turtle. Flagellates were found in ranid frogs and the Eastern American toad Bufo a. americanus, based on one study. The rest of the protozoan species, such as Nyctotherus cordiformis, were reported from ranid frogs, while the coccidian species Eimeria longaspora and Eimeria megaresidua were reported from the eastern newt Notophthalmus viridescens. Thirty-nine species of adult digenetic trematodes from 13 families have been reported in Michigan herps (Table 1). A total of 19 digenetic trematode species have been found in amphibians (18 in frogs, 2 in toads, 5 in salamanders), 8 species in snakes, 15 species in turtles, and 1 species has been found in both a frog and a turtle. Regarding trematode families, members of the Brachycoelidae and Cephalogonimidae infect amphibians; Gorgoderidae, Haematoloechidae, Hemiuridae, and Lecithodendriidae primarily infect ranid frogs; Macroderoididae and Paramphistomidae (except for Allassostomoides parvum) primarily infect hylid and ranid frogs; Plagiorchiidae infect snakes and turtles; Pronocephalidae infect turtles and a frog; Heronimidae and Spirorchiidae infect turtles; and Telorchiidae primarily infect turtles. The families Haematoloechidae and Plagiorchiidae are 2

6 represented by six and seven species, respectively, and the Spirorchiidae and Telorchiidae each have five species. At least 12 different species of larval digenetic trematodes representing 7 families have been reported from herps in Michigan (Table 1). Most species infect amphibians (11 in frogs, 1 in toads, 4 species in salamanders). Only larval Alaria intermedia, Alaria marcianae, and mesocercaria (=Alaria) have been reported from snakes. Only one larval trematode (Cercaria welleri) has been reported from turtles. Adult cestodes in three families have been reported from amphibians in Michigan with Bothriocephalus rarus infecting Notophthalmus viridescens, Cylindrotaenia americana and Cylindrotaenia quadrijugosa infecting the northern leopard frog Rana pipiens, and Proteocephalus saphena infecting green frogs Rana clamitans melanota (Table 1). The one report of Proteocephalus sp. infecting the tiger salamander Ambystoma t. tigrinum and ranid frogs involves non-gravid worms. Only one cestode species (Proteocephalus perspicua) has been reported from snakes. Larvae of two genera of cestodes (Mesocestoides and Proteocephalus) infect ranid frogs. Cestodes have not been reported from turtles. Adults of at least 15 nematode species in 10 families have been reported from herps in Michigan (Table 1). Eleven species infect amphibians with most of them in ranid frogs and three species occur in salamanders. Thelandros magnavulvaris only infects salamanders. Adult Camallanus microcephalus, Spiroxys amydae, and Spiroxys contortus have been reported from turtles. Dracunculus ophidensis, Rhabdias fuscovenosa, unidentified adults, and microfilariae (larvae) have been found in snakes. Encysted larval Spiroxys sp. are common nematodes of amphibians. The parasites found in amphibians and reptiles in Michigan by herp order are listed in Table 2. Six species of salamanders in three families have parasites reported from them. Seven parasite species from three studies have been reported from the blue-spotted salamander Ambystoma laterale. The spotted salamander Ambystoma maculatum and eastern tiger salamander Ambystoma t. tigrinum each have only had one study on their parasites. Eight studies have been performed on the parasites of Notophthalmus viridescens from Michigan. Five of the 11 species infecting newts are digenetic trematodes. Only one study was done on the parasites of the red-backed salamander Plethodon cinereus. Seven studies have been performed on the protozoan species Cepedietta michiganensis infecting the four-toed salamander Hemidactylium scutatum. Five studies have been performed on the parasites of toads with most studies involving Bufo a. americanus. Six parasite species (four protozoans, two digeneans) have been reported from this toad species. The digenetic trematode Cephalogonimus americanus is the only species reported from the Fowler s toad Bufo fowleri in one study. Twelve parasite species from eight studies have been reported from four hylid frog species. Ten species of parasites have been reported from the northern spring peeper Pseudacris c. crucifer and four species from the striped chorus frog Pseudacris triseriata. Only one parasite species has been reported from Blanchard s cricket frog Acris crepitans blanchardi and one from the eastern gray treefrog Hyla versicolor. Eighteen species of parasites from nine studies have been reported from Rana catesbeiana. Twenty-eight studies have been performed on green frog parasites with 43 parasite species listed. Twenty-three species are digenetic trematodes with 15 of these being adults and 8 species are larvae. Three cestode species and 10 nematode species are reported from green frogs. Thirty studies have been performed on the parasites of the northern leopard frog Rana pipiens with at least 31 parasite species listed. At least nine of these species are represented as larval trematodes and six species are adult trematodes. Only one study has been published on the parasites of each of the pickerel frog Rana palustris and of the mink frog Rana septentrionalis, and this last one only involved the blood. Eight studies listing 14 parasite species have been done on wood frogs; 7 of these species are digenetic trematodes. Tadpoles of the following anuran species have been found infected with parasites (in parentheses): Bufo a. americanus (Cephalogonimus americanus), Bufo fowleri (C. americanus), Bufo sp. (C. americanus), 3

7 Rana catesbeiana (Halipegus eccentricus), Rana c. melanota (Alaria marcianae, Alaria mustelae, Caudorchis eurinus, C. americanus, Diplostomum micradenum, Echinoparyphium flexum, H. eccentricus, Lechriorchis primus, Megalodiscus temperatus, trematode cysts, Proteocephalus perspicua, Proteocephalus saphena, Spiroxys contortus, Spiroxys sp.); Rana pipiens (A. marcianae, Alaria intermedia, A. mustelae, Apharyngostrigea pipientis, C. eurinus, D. micradenum, E. flexum, H. eccentricus, L. primus, gorgoderids); Rana sylvatica (E. flexum); Pseudacris c. crucifer (E. flexum); Pseudacris triseriata (E. flexum); Hyla versicolor (A. pipientis); species not given (Ribeiroa ondatrae, D. micradenum, Cercorchis medius, Telorchis medius). Parasites found in the following larval caudates are: Notophthalmus viridescens (Bothriocephalus rarus); Ambystoma maculatum (C. americanus); Ambystoma t. tigrinum (Telorchis corti, Diplostomum sp., Proteocephalus sp.). All these helminth species occurring in tadpoles and larval caudates were larval or immature stages except for T. corti that was represented by some gravid stages. Eight species of snakes in one family from Michigan have parasites reported from them. At least 10 parasite species occur in the northern water snake Nerodia s. sipedon based on 8 studies. The northern ribbon snake Thamnophis sauritus septentrionalis and the common garter snake Thamnophis sirtalis have five and eight species reported from them, respectively. The other snake species (brown snake Storeria dekayi, northern red-bellied snake Storeria o. occipitomaculata, northern ring-necked snake Diadophis punctatus edwardsi, eastern milk snake Lampropeltis t. triangulum, eastern smooth green snake Opheodrys vernalis) had one to three species reported from them involving three studies or less. All snake species infected with Entamoeba invadens involved experimental infections in the laboratory. These snakes were caught in the Douglas Lake area of Michigan. Wild snakes in Michigan have not been found infected with E. invadens. Eight species of turtles in four families have parasites reported from them in Michigan. Spiroxys contortus infected all these species. The painted turtle Chrysemys picta had 18 parasite species (13 of which are digenetic trematodes) reported from it involving 14 studies. Three studies on the parasites of the eastern spiny softshell turtle Apalone s. spinifera reported five parasite species. Digenetic trematodes have been found in four turtle species. Of the turtle species, the painted turtle is the only one infected with a larval trematode. Of all the herp species examined from Michigan, the painted turtle is the only one infected with monogeneans. The sites occupied by parasites in Michigan amphibians and reptiles by host order are in Table 3. At least 11 species of parasites occur in the digestive tract of salamanders from Michigan with 8 of these species reported from the intestine. The gall bladder, lung, blood, and lens of the eye each harbored one parasite species. Five species of larval parasites occurred elsewhere in the body. At least 23 species of parasites have been reported from the digestive tract of anurans in Michigan. Eight species infect the lungs and at least four species have been found in the urinary bladder and kidneys. Six Trypanosoma spp. have been found in the blood. Larval and immature parasites of all the parasite groups except the monogeneans occur unencysted or encysted in the body cavity, extra intestinal visceral organs, and muscles. Most parasites reported from Michigan snakes are from the digestive tract and lungs. Five parasite species are reported from the blood of turtles, four species from the digestive tract, and one species from the lungs. The sites of several species infecting turtles were not given in the original articles. Published studies on the parasites of herps have been performed in 13 counties of Michigan. At least 45 studies occurred in Cheboygan County from 1916 through 1968, due to the investigations of parasitologists at the University of Michigan Biological Station at Douglas Lake. Washtenaw County has had at least 17 studies. Specific locations of six studies in Michigan were not reported. Only two articles have been published on the parasites of herps in the Upper Peninsula. One of these involved the occurrence of Cephalogonimus americanus in Rana c. melanota and the other listed blood flagellates found in six species of anurans. The number of studies (in parentheses) published on the parasites of herps in Michigan 4

8 in 20-year intervals were: (11), (43), (19), (2), and after 1990 (9). Most studies (35) were published from 1930 through Discussion A survey of the literature on the parasites of herps in Michigan reveals that most articles deal with parasite life histories and taxonomy, and parasite surveys of one or more herp species. These studies were not warranted by some pressing or continuous issue involving parasite or herp biology or pathology, but represent the interests of specific investigators. At least 84 studies have been published on some aspect of parasites infecting Michigan herps. Of these studies, 49 involve frogs, 5 involve toads, 19 involve salamanders, 15 involve snakes, and 16 involve turtles. These numbers are inflated because some abstracts and articles by a few authors involve the same parasites and hosts. Many articles present data on the prevalence (percentage of a herp species infected with a parasite species), mean intensity (mean number of parasites per infected herp), and mean abundance (mean number of parasites per examined herp). A few articles include information on the diversity of the helminth fauna of a herp species. More parasite species have been found in amphibians, primarily anurans, than in reptiles because more studies have examined their parasites, and more amphibian species and greater numbers of them have been examined. None of the parasites species reported from Michigan herps are exotic species. A few species of helminths (e.g., Clinostomum sp., Diplostomum sp., Ribeiroia ondatrae, Proteocephalus sp., Camallanus sp., Spinitectus gracilis, and Spiroxys sp.) found in Michigan amphibians also infect fish. Gravid S. gracilis have been found in both ranid frogs and centrarchid fish. Larval R. ondatrae occur in both tadpoles and fish. Larval Clinostomum sp., Diplostomum sp., Proteocephalus sp., Camallanus sp., and Spiroxys sp. infect amphibians and fish in Michigan but it is not known if infections in these animals involve the same helminth species. The total numbers of parasite species found in each herp group in parentheses are: salamanders (19), toads (7), hylid frogs (12), ranid frogs (at least 50), snakes (15), and turtles (22). Overall, both toads and hylid frogs were infected with two parasite groups: toads (protozoans 57%; trematodes, 43%) and hylid frogs (trematodes 67%; nematodes, 33%). The percentages (in parentheses) of each parasite group (protozoans, trematodes, monogeneans, cestodes, and nematodes, respectively) for the remaining herp groups are: salamanders (21%, 47%, 0%, 11%, 21%), ranid frogs (13%, 57%, 0%, 11%, 19%), snakes (27%, 53%, 0%, 7%, 13%), and turtles (5%, 71%, 10%, 0%, 14%). Excluding toads, trematodes are the most common parasites found in the herp groups. Monogeneans have only been reported from turtles. Cestodes have not been found in toads, hylid frogs, and turtles. As more studies are performed on herp species (groups) in Michigan, more parasite species will be found. Earlier it was mentioned that no attempt was made to demonstrate the past complexities of parasite synonyms. However, it should be pointed out that a few helminth species in some families such as Haematoloechidae, Spirorchiidae, Telorchiidae, and Molineidae have undergone name revisions and synonymizations. Therefore, the taxonomic status of some species listed in the tables in this review article may be uncertain. Several investigators have suggested there is a positive correlation between type of habitat occupied by the herp species and number of helminth species found, with those species associated with aquatic environments having more parasite species than terrestrial ones. Most parasite species reported from herps in Michigan are digenetic trematodes that utilize molluscs as intermediate hosts. The presence of more parasite species in frogs compared to other herp groups in Michigan is likely due to their association with aquatic habitats. Frogs eat many aquatic organisms that serve as intermediate hosts for digenetic trematodes and other parasite groups, and live in the water where larval parasites (primarily trematodes) can directly penetrate and infect them. Other explanations may be that snakes and turtles in Michigan have not been surveyed for their parasites as commonly as frogs, or parasites may 5

9 not be that common in Michigan snakes and turtles. Herps may be infected with either the larval or adult stage of the parasite species and can serve as either the intermediate or definitive host or both at the same time. In many cases, the predator-prey relationships of herps help explain the transmission of the parasites that infect them. Frogs are infected with many species of larval parasites indicating they serve as intermediate hosts for several parasites and are eaten by several species of predators. Not enough studies in Michigan have been performed on toads, salamanders, snakes, and turtles to determine if they have many larval parasites. Many herp species in Michigan serve as definitive hosts for several parasite species that they acquire by eating intermediate hosts. Where the parasitological data comparing herp developmental stages are known, more parasite species have been found in adult frogs compared to tadpoles or juveniles. An increase in the number of parasite species and their numbers in adults can be a function of time, with older (larger) individuals having a longer time to acquire parasites, or reflect ontogenetic shifts in diet, habitat, or behavior. Studies on the parasites of herps sometimes offer some interesting insights on how they affect their hosts. Two examples in Michigan will suffice. Brackett (1938) reported that gravid females of the nematode Dracunculus ophidensis are found primarily on the dorsal surface of the snake Thamnophis sirtalis, producing dermal elevations characteristic of infection. Brackett (1938) stated The remains of a female worm which has given off its larvae are in some way disposed of by the snake s tissue, for all traces of the infection disappear by fall or early winter. In a letter from Bruce Lang regarding D. ophidensis infecting T. sirtalis, it was stated The snake s tail is damaged to the point where portions drop off when an infection forms in the area around the blister where the larvae exit the snake. And furthermore This then could explain the high percentage of T. sirtalis with portions of their tail missing in the Cheboygan area of Michigan. Cort and Brackett (1938) reported that the unencysted larval diplostomula stages of the trematode, Cercaria ranae, occurred in the body cavity and are widely distributed in the tissues of tadpoles. They reported that heavy infections in the tadpoles caused severe symptoms, producing a condition that they called bloat disease, due to the characteristic distension of the abdomen. Studies have not been published on the parasites of mudpuppies Necturus maculosus maculosus, western lesser sirens Siren intermedia nettingi, marbled salamanders Ambystoma opacum, small-mouthed salamanders Ambystoma texanum, Cope s gray treefrog Hyla chrysoscelis, Kirtland s snake Clonophis kirtlandii, northern copper-bellied water snake Nerodia erythrogaster neglecta, queen snake Regina septemvittata, Butler s garter snake Thamnophis butleri, eastern hognose snake Heterodon platyrhinos, racer Coluber constrictor foxi, black rat snake Elaphe obsoleta obsoleta, eastern fox snake Elaphe gloydi, western fox snake Elaphe vulpina, eastern massasauga rattlesnake Sistrurus catenatus catenatus, wood turtle Glyptemys insculpta, red-eared slider Trachemys scripta elegans, five-lined skink Eumeces fasciatus, and six-lined racerunner Cnemidophorus sexlineatus, in Michigan. Fowler s toad, Blanchard s cricket frog, eastern gray treefrog, pickerel frog, mink frog, spotted salamander, eastern tiger salamander, red-backed salamander, brown snake, northern red-bellied snake, northern ringnecked snake, common musk turtle, spotted turtle, eastern box turtle, and Blanding s turtle each have had only one study published on their parasites. Furthermore, before the anecdotal report of Muzzall et al. (2001) of Pneumatophilus foliaformis infecting Nerodia s. sipedon, the last publication on the parasites of snakes in Michigan was Yongue (1964). Also, the last report of a parasite infecting a turtle in Michigan was the brief mention by Esch and Kocan (1966). The lack of parasitological studies on these herp species and the infrequency of studies on other species in Michigan are not surprising and are due to several reasons. These include: the distributions of some herp species in Michigan are restricted; some species occur in low numbers; some species are threatened or endangered; lack of interest by investigators; and lack of financial support for studies like this. Parasites can be found in all the organs of a herp. If only the digestive tract of the herp is examined, some parasite species (and their 6

10 numbers), as indicated by this review, would be missed and not counted. There may be hundreds of larval parasites in the herp. Many of the larval digenetic trematodes, cestodes, and nematodes infecting herps (especially amphibians) in Michigan are difficult to work with because removing larvae from their cysts may be difficult. If successfully removed, they should be examined alive to find characteristics, if developed enough, that will be useful for identification. Larval parasites may also be identified to species if feeding experiments of the larvae are performed and adult worms are found in the animals that were fed the larvae. There are a few terms that describe various larval stages of trematodes and cestodes that occur in herps, primarily amphibians, that deserve mention for clarification purposes. Several species of cercariae have been described and illustrated in the older literature, being given the generic name Cercaria for these species. Therefore, the scientific name of these digenetic trematodes may not be known. Thus, the term cercaria has been used as a generic name, and more appropriately as a common name for certain larval stages of digenetic trematodes. Bosma (1934) used the terms, immature metacercaria and agamodistomum to define the larval trematode stage that forms from the cercaria that penetrates into and occurs in tadpoles and frogs of the trematode genus Alaria. She demonstrated by experiments that the so-called agamodistomum of Alaria mustelae is an essential step in the development of the next larval stage called the metacercaria. She suggested that the name mesocercaria should be used instead of immature metacercaria or agamodistomum. In support of this, Olivier and Odlaug (1938) employed mesocercaria (sometimes referred to as the genus Mesocercaria (=Agamodistomum) in the earlier literature) as the name for these stages of trematodes with four-host life cycles. The latter authors found mesocercaria of Alaria intermedia (=Mesocercaria intermedia) in the muscles and pericardial region of tadpoles and adult Rana pipiens and in the fatty tissue of the tail of Thamnophis sirtalis. Therefore, unencysted mesocercaria can be found in both amphibians and reptiles. Schell (1985) reported that the mesocercaria stage can also be produced by digenetic trematodes in the genera Procyotrema, Pharyngostomoides, and Strigea. In general, larval cestodes can be recognized by the presence of calcareous corpuscles. Larval cestodes generally referred to as tetrathyridia may be found and are considered to be of the genus Mesocestoides. These stages have a deeply invaginated and inverted unarmed scolex with four suckers. Schmidt (1970) defined a tetrathyridium as the cysticercoid of Mesocestoides that has a solid body and a scolex not surrounded by special membranes. A juvenile cestode in its host can also be called a metacestode. Johnson et al. (2002) reviewed information on larval trematodes producing deformities in amphibians in North America. They reported that the larval trematode Ribeiroia ondatrae was associated with, and functionally related to, higher frequencies of amphibian limb malformations than found in uninfected populations. Gillilland and Muzzall (2002) reported on the larval helminth parasites infecting amphibians from southern Michigan and discussed the lack of deformities in them from this area. The earliest article on the larval trematodes of amphibians in Michigan was Cort (1918). Although all the animal species (snails, amphibians and fish, herons, and hawks) necessary for the completion of the life cycle of R. ondatrae occur in Michigan, limb malformations of amphibians and the relationship between larval trematodes and amphibian malformations were never mentioned in articles on the larval trematodes of Michigan amphibians. If R. ondatrae can produce limb malformations in amphibians, might it also be possible that larval cestodes and nematodes can cause deformities. In Michigan and elsewhere, unencysted and encysted larval cestodes and nematodes are common parasites of amphibians but so far, a relationship between these larval helminths and deformities has not been reported. Beaver (1939) reported on the occurrence of metacercariae of Ribeiroia ( = Psilostomum) ondatrae in the lateral line canal and under the scales of freshwater fish (experimental and field infections) from Douglas Lake, Michigan and the surrounding region. He stated that metacercariae also develop in the nostrils of tadpoles and fish, and occasionally may be found in the cloaca and associated ducts after 7

11 prolonged exposure to heavy suspensions of cercariae and that Never more than a dozen or so would encyst in any one of these small hosts, however. He also mentioned that adult R. ondatrae were found in Cooper s Hawks and that laboratory infections were obtained in other birds. Since the study by Beaver (1939), R. ondatrae has not been reported from Michigan herps. Dyer (1991) did not list Ribeiroia occurring in amphibians from Illinois and adjacent states. Several articles and reports have mentioned that some species of herps in the world have declined and other species showed no decline in their numbers. Apparently there is no single factor or set of factors that can be presented to explain these declines. However, habitat destruction, general environmental degradation, and exploitation of herps serving as food items were implicated in many instances. It is important to point out that if herp species are declining, and if one or more of their parasite species are host specific, then parasites are also declining. The parasites of herps should not be overlooked and their influence on herps should not be underestimated. Johnson et al. (2002) and Daszak et al. (2003) demonstrated their importance in causing amphibian deformities and reducing their population numbers at some locations. I recommend that if individuals are removed from a herp population to be studied for various purposes, they should also be examined for parasites. A multidisciplinary approach to studying herp populations is essential to understand all aspects of the biology of the herp species being examined. Acknowledgments I kindly thank Matt Bolek, School of Biological Sciences, University of Nebraska Lincoln; Jim Harding, Department of Zoology, Michigan State University; and Gary Whelan, Michigan Department of Natural Resources for reading an early draft of this manuscript. I also thank Jim Harding for providing the letter from Bruce Lang on Dracunculus ophidensis. 8

12 Table 1. List of parasites reported in amphibians and reptiles from Michigan. The classification of parasites is partly based on that of Baker (1987) and Yamaguti (1959, 1971). References in parentheses following hosts refer to references for host records. Sarcodina (Ameba): Entamoebidae Chatton, 1925 Entamoeba invadens Rodhain, 1934 Host: Diadophis punctatus edwardsii, Lampropeltis t. triangulum, Nerodia s. sipedon, Opheodrys vernalis, Storeria dekayi, Storeria o. occiptomaculata Thamnophis sauritus septentrionalis, Thamnophis sirtalis, (Barrow and Stockton 1960). Mastigophora (Flagellates): Hexamitidae Kent Octomitus intestinalis Dujardin Host: Rana clamitans melanota, Rana pipiens, (Fortner 1923). Opalinidae Claus, 1874 Opalina obtrigonoidea Metcalf Host: Rana c. melanota, Rana pipiens, Rana sylvatica, (Fortner 1923). Trichomonadidae Chalmus and Pekkola, 1918 Trichomonas sp. Donne, 1836 Host: Nerodia s. sipedon, (Barrow and Stockton 1960). Trypanosomatidae Doflein, 1901 Trypanosoma bufophlebotomi Ayala, 1970 Host: Bufo a. americanus, (Werner and Walewski 1976). Trypanosoma diemictyli Tobey, 1906 Host: Notophthalmus viridescens, (Werner and Walewski 1976). Trypanosoma pipientis Diamond, 1950 Host: Rana c. melanota, Rana pipiens, (Werner and Walewski 1976). Trypanosoma pseudopodium Werner and Walewski, 1976 Host: Bufo a. americanus, (Werner and Walewski 1976). Trypanosoma ranarum (Lankester, 1871) Danilewsky 1885 Host: Rana catesbeiana, Rana c. melanota, Rana pipiens, Rana septentrionalis, Rana sylvatica, (Werner and Walewski 1976). Trypanosoma rotatorium (Mayer, 1843) Laveran and Mesnil 1901 Host: Rana catesbeiana, Rana c. melanota, Rana pipiens, Rana septentrionalis, (Werner and Walewski 1976). Trypanosoma schmidti-like species Diamond, 1965 Host: Bufo a. americanus, (Werner and Walewski 1976). Ciliophora (Ciliates): Haptophyridae Cepede, 1910 Cepedietta michiganenesis Woodhead, 1928 Host: Ambystoma laterale, (McIntosh 1935; Woodhead 1928); Plethodon cinereus, (Muzzall 1990); Hemidactylium scutatum, (Blanchard 1923; Bush 1934; MacLennan 1944; McIntosh 1935; Rankin 1938; Woodhead 1928; Woodhead and Kruidenier 1936); Bufo a. americanus, (McIntosh 1935); Rana c. melanota, (Muzzall et al. 2001). Nyctotheridae Amaro, 1972 Nyctotherus cordiformis Ehrenberg Host: Rana c. melanota, Rana pipiens, (Fortner 1923). 9

13 Table 1 Continued. Apicomplexa (Apicomplexans): Eimeriidae Minchin, 1903 Eimeria longaspora Barrow and Hoy, 1960 Host: Notophthalmus viridescens, (Barrow and Hoy 1960). Eimeria megaresidua Barrow and Hoy, 1960 Host: Notophthalmus viridescens, (Barrow and Hoy 1960). Coccidians Host: Thamnophis sauritus septentrionalis, (Barrow and Stockton 1960). Plasmodiidae Mesnil, 1903 Haemoproteus metchinikovi (Simond, 1901) Host: Chrysemys picta, (DeGiusti and Batten 1951). Haemogregarine-like form Host: Nerodia s. sipedon, (Yongue 1964). Unidentified protozoans Host: Rana sylvatica, (Woodhams et al. 2000). Adult Digenea (Digenetic Trematodes): Brachycoeliidae Johnston, 1912 Brachycoelium salamandrae (Froelich, 1789) Host: Ambystoma laterale, (Muzzall and Schinderle 1992); Plethodon cinereus, (Muzzall 1990); Acris crepitans blanchardi, (Najarian 1955); Rana sylvatica, (Najarian 1955). Brachycoelium sp. Stiles and Hassall, 1898 Host: Hemidactylium scutatum, (Rankin 1938). Cephalogonimidae Nicoll, 1915 Cephalogonimus americanus Stafford, 1902 Host: Ambystoma maculatum, (Lang 1968); Bufo fowleri, (Lang 1968); Bufo sp., (Lang 1968); Rana c. melanota, (Fortner 1923; Lang 1968; Najarian 1955; Spence and Peters 1971); Rana pipiens, (Fortner 1923; Najarian 1955). Cephalogonimus vesicaudus Nickerson, 1912 Host: Rana c. melanota, (Najarian 1955). Gorgoderidae Looss, 1901 Gorgodera amplicava Looss, 1899 Host: Rana c. melanota, (Muzzall 1991b; Muzzall et al. 2001; Najarian 1955). Gorgoderina attenuata (Stafford, 1902) Stafford, 1905 Host: Rana catesbeiana, (Muzzall 1991b); Rana c. melanota, (Fortner 1923; Muzzall 1991b; Muzzall et al. 2001); Rana pipiens, (Fortner 1923). Gorgoderina simplex (Looss, 1899) Looss, 1902 Host: Rana catesbeiana, Rana c. melanota, (Najarian 1955). Juvenile gorgoderids Host: Rana pipiens, (Goodchild 1950). Haematoloechidae Odening, 1964 Haematoloechus breviplexus Stafford, 1902 Host: Rana c. melanota, (Najarian 1955). Haematoloechus longiplexus Stafford, 1902 Host: Rana catesbeiana, (Krull 1932; Muzzall 1991b; Najarian 1955); Rana c. melanota, (Muzzall 1991b). Haematoloechus medioplexus Stafford, 1902 Host Bufo a. americanus, (Krull 1931); Rana c. melanota, (Fortner 1923); Rana pipiens, (Fortner 1923; Krull 1930; Krull 1931). 10

14 Table 1 Continued. Haematoloechus parviplexus (Irwin, 1929) Host: Rana catesbeiana, (Muzzall 1991b); Rana c. melanota, (Krull 1930; Krull 1931; Muzzall 1991b; Najarian 1955); Rana sylvatica, (Muzzall and Peebles 1991). Haematoloechus similiplexus Stafford, 1902 Host: Rana c. melanota, Rana pipiens, (Fortner 1923). Haematoloechus varioplexus Stafford, 1902 Host: Rana c. melanota, (Muzzall et al. 2001); Rana sylvatica, (Najarian 1955). Hemiuridae Luhe, 1901 Halipegus eccentricus Thomas, 1939 Host: Rana catesbeiana, Rana pipiens, (Thomas 1939); Rana c. melanota, (Ameel et al. 1949; Muzzall et al. 2001; Thomas 1939). Halipegus sp. Looss, 1899 Host: Notophthalmus viridescens, (Muzzall 1991a); Rana catesbeiana, (Muzzall 1991b); Rana c. melanota, (Krull 1935; Muzzall 1991b). Heronimidae Ward, 1917 Heronimus chelydrae MacCallum, 1902 Host: Chrysemys picta, (Ward 1917; Esch and Gibbons 1967). Lecithodendriidae Odhner, 1910 Loxogenes arcanum (Nickerson, 1900) Stafford, 1905 Host: Rana catesbeiana, (Muzzall 1991b); Rana c. melanota, (Muzzall 1991b; Spence and Peters 1971). Macroderoididae McMullen, 1937 Glypthelmins pennsylvaniensis Cheng, 1961 Host: Pseudacris c. crucifer, (Muzzall and Peebles 1991); Pseudacris triseriata, (Muzzall and Peebles 1991). Glypthelmins quieta (Stafford, 1900) Stafford, 1905 Host: Pseudacris c. crucifer, (Najarian 1955); Rana catesbeiana, (Muzzall 1991b; Najarian 1955); Rana c. melanota, (Muzzall 1991b; Muzzall et al. 2001; Najarian 1955); Rana sylvatica, (Muzzall and Peebles 1991). Paramphistomidae Fischoeder, 1901 Allassostomoides parvum (Stunkard, 1916) Travassos, 1934 Host: Chrysemys picta, (Esch and Gibbons 1967). Megalodiscus temperatus (Stafford, 1905) Harwood, 1932 Host: Notophthalmus viridescens, (Muzzall 1991a; Muzzall et al. 2003); Pseudacris c. crucifer, (Herber 1939; Najarian 1955); Rana catesbeiana, (Krull and Price 1932; Muzzall 1991b; Najarian 1955); Rana c. melanota, (Fortner 1923; Krull and Price 1932; Muzzall 1991b; Muzzall et al. 2001; Najarian 1955); Rana pipiens, (Fortner 1923; Krull and Price 1932; Van der Woude 1954); Rana sylvatica, (Krull and Price 1932; Van der Woude 1954). Plagiorchiidae Ward, 1917 Eustomos chelydrae MacCallum, 1921 Host: Chelydra s. serpentina, (McMullen 1935); Chrysemys picta, (Esch and Gibbons 1967; McMullen 1935). Lechriorchis primus Stafford, 1905 Host: Thamnophis s. septentrionalis, (Cort et al. 1952); Thamnophis sirtalis, (Cort et al. 1952). Natriodera verlata (Talbot, 1934) Host: Nerodia s. sipedon, (Talbot 1934). Pneumatophilus foliaformis Talbot, 1934 Host: Nerodia s. sipedon, (Muzzall et al 2001; Talbot 1934). 11

15 Table 1. Continued. Renifer orula (Talbot, 1934) Host: Nerodia s. sipedon, (Talbot 1934). Zeugorchis eurinus (Talbot, 1933) Host: Thamnophis s. septentrionalis, Thamnophis sirtalis, (Talbot 1933). Zeugorchis megametricum (Talbot, 1934) Host: Thamnophis sirtalis, (Talbot 1934). Pronocephalidae Looss, 1902 Macravestibulum eversum Hsu, 1937 Host: Graptemys geographica, (Hsu 1937). Teloporia aspidonectes (MacCallum, 1917) Fukui, 1933 Host: Rana catesbeiana, Apalone s. spinifera, (Esch and Kocan 1966). Spirorchiidae Stunkard, 1921 Spirorchis artericola (Ward, 1921) Host: Chrysemys picta, (Esch and Gibbons 1967). Spirorchis elephantis (Cort, 1917) Host: Chrysemys picta, (Wall 1941b). Spirorchis parvus (Stunkard, 1923) Host: Chrysemys picta, (Wall 1940; Wall 1941a). Spirorchis sp. MacCallum, 1919 Host: Chrysemys picta, (Cort et al. 1954; Wall 1939). Vasotrema amydae (Stunkard, 1926) Host: Apalone s. spinifera, (Wall 1951). Vasotrema robustum Stunkard, 1928 Host: Apalone s. spinifera, (Wall 1951). Telorchiidae Stunkard, 1924 Protenes angustus (Stafford, 1900) Ward, 1918 Host: Chrysemys picta, (Esch and Gibbons 1967). Telorchis attenuatus Goldberger, 1911 Host: Chrysemys picta, (Esch and Gibbons 1967). Telorchis corti Stunkard, 1915 Host: Notophthalmus viridescens, (Muzzall 1991a); Ambystoma t. tigrinum, (Muzzall and Schinderle 1992); Chrysemys picta, (Esch and Gibbons 1967). Telorchis diminutis Stunkard, 1915 Host: Chrysemys picta, (Esch and Gibbons 1967). Telorchis medius Stunkard, 1915 Host: tadpoles, Chrysemys picta, Thamnophis spp., (McMullen 1934). Larval Digenea (Digenetic Trematodes): Clinostomidae Luhe, 1901 Clinostomum attenuatum Cort, 1913 Host: Rana c. melanota, (Fortner 1923; Najarian 1955); Rana pipiens, (Fortner 1923). Clinostomum sp. Leidy, 1856 Host: Notophthalmus viridescens, (Muzzall 1991a); Rana catesbeiana, (Muzzall 1991b); Rana c. melanota, (Muzzall et al. 2001); Rana pipiens, (Gillilland and Muzzall 1999). Diplostomidae Poirier, 1886 Diplostomum micradenum Olivier, 1940 Host: Bufo a. americanus, Pseudacris c. crucifer, Rana c. melanota, Rana pipiens, (Olivier 1938; Olivier 1940); Rana pipiens, (Olivier 1942). 12

16 Table 1. Continued. Diplostomum sp. Nordmann, 1832 Host: Ambystoma t. tigrinum, (Muzzall and Schinderle 1992). Fibricola sp. Dubois, 1932 Host: Rana c. melanota, (Muzzall et al. 2001); Rana pipiens, (Gillilland and Muzzall 1999). Echinostomatidae Poche, 1926 Echinoparyphium flexum (Linton, 1892) Dietz, 1910 Host: Pseudacris c. crucifer, Pseudacris triseriata, Rana c. melanota, Rana pipiens, Rana sylvatica, (Najarian 1952; Najarian 1953a; Najarian 1954); Rana pipiens, (Najarian 1953b). Echinostome metacercariae Host: Ambystoma laterale, (Muzzall and Schinderle 1992); Pseudacris c. crucifer, (Najarian 1955); Rana c. melanota, (Muzzall et al. 2001; Najarian 1955); Rana sylvatica, (Najarian 1955). Gorgoderidae Looss, 1901 Gorgoderid metacercariae Host: Pseudacris c. crucifer, (Najarian 1955); Rana c. melanota, (Muzzall et al. 2001; Najarian 1955); Rana sylvatica, (Najarian 1955). Plagiorchiidae Ward, 1917 Lechriorchis primus Stafford, 1905 Host: Rana c. melanota, Rana pipiens, (Talbot 1933). Renifer metacercariae Host: Rana pipiens, (Najarian 1955). Immature plagiorchids Host: Rana pipiens, (Gillilland and Muzzall 1999). Psilostomatidae Odhner, 1913 Ribeiroia ondatrae (Price, 1931) Host: unspecified tadpoles, (Beaver 1939). Strigeidae Railliet, 1919 Alaria intermedia Olivier and Odlaug, 1938 Host: Rana pipiens, Thamnophis sirtalis, (Olivier and Odlaug 1938). Alaria marcianae (La Rue 1917) Host: Rana c. melanota, Rana pipiens, (Cort 1918); Thamnophis sirtalis, (Cort 1918; Cort and Brooks 1928); Nerodia s. sipedon, (Cort and Brooks 1928). Alaria mustelae Bosma 1925 Host: Rana catesbeiana, Rana c. melanota, Rana palustris, Rana pipiens, (Bosma 1934); unidentified frogs, (Bosma 1925). Apharyngostrigea pipientis (Faust, 1918) Host: Hyla versicolor, Rana pipiens, (Hughes 1928; Olivier 1939). Strigeid metacercariae Host: Rana pipiens, (Gillilland and Muzzall 1999). Mesocercaria Host: Nerodia s. sipedon, (Yongue 1964). Cercaria ranae Host: Rana pipiens, (Cort and Brackett 1937; Cort and Brackett 1938). Cercaria welleri McMullen, 1938 Hosts: Chelydra sp., Chrysemys sp., Nerodia sp., (McMullen 1938). Metacercariae A Host: Notophthalmus viridescens, (Muzzall et al. 2003); Rana c. melanota, (Muzzall et al. 2001). 13

17 Table 1. Continued. Unidentified metacercariae Host: Ambystoma laterale, (Muzzall and Schinderle 1992); Rana pipiens, (Gillilland and Muzzall 1999); Rana sylvatica, (Muzzall and Peebles 1991; Woodhams et al. 2000). Adult Monogenea (Monogeneans): Polystomatidae Gamble, 1896 Neopolystoma orbiculare (Stunkard, 1916) Price, 1939 Host: Chrysemys picta, (Esch and Gibbons 1967). Polystomoides coronatum (Leidy, 1888) Ozaki, 1935 Host: Chrysemys picta, (Bychowsky 1961; Esch and Gibbons 1967). Adult Cestoda (Cestodes): Bothriocephalidae Blanchard, 1849 Bothriocephalus rarus Thomas, 1937 Host: Notophthalmus viridescens, (Muzzall 1991a; Thomas 1927; Thomas 1934; Thomas 1937a; Thomas 1937b). Nematotaeniidae Luhe, 1910 Cylindrotaenia americana Jewell, 1916 Host: Rana pipiens, (Jewell 1916). Cylindrotaenia quadrijugosa Lawler, 1939 Host: Rana pipiens, (Lawler 1939). Proteocephalidae La Rue, 1911 Proteocephalus perspicua La Rue, 1911 Host: Nerodia s. sipedon, (Thomas 1941). Proteocephalus saphena Osler, 1931 Host: Rana c. melanota, (Muzzall et al. 2001; Osler 1931; Thomas 1931). Proteocephalus sp. Weinland, 1858 Host: Ambystoma t. tigrinum, (Muzzall and Schinderle 1992); Rana c. melanota, (Muzzall 1991b). Proteocephalidae La Rue, 1911 Host: Rana c. melanota, Rana pipiens, (Fortner 1923). Larval Cestoda (Cestodes): Mesocestoididae Perrier, 1897 Mesocestoides sp. Vaillant, 1863 Host: Rana c. melanota, (Muzzall et al 2001); Rana pipiens, (Gillilland and Muzzall 1999); Rana sylvatica, (Woodhams et al. 2000). Proteocephalidae La Rue, 1911 Proteocephalus perspicua La Rue, 1911 Host: Rana c. melanota, (Thomas 1941). Proteocephalus sp. Weiland 1858 Host: Rana c. melanota, (Muzzall et al. 2001). Adult Nematoda (Nematodes): Camallanidae Railliet and Henry, 1915 Camallanus microcephalus (Dujardin, 1845) (Railliet and Henry, 1915) Host: Chrysemys picta, (Esch and Gibbons 1967). Camallanus sp. Railliet and Henry, 1915 Host: Rana c. melanota, (Muzzall et al. 2001). Serpinema sp. Yeh, 1960 Host: Rana c. melanota, (Muzzall 1991b). 14

18 Table 1. Continued. Cosmocercidae (Railliet, 1916) Travassos, 1925 Cosmocercoides dukae (Holl, 1928) Travassos, 1931 Host: Pseudacris triseriata, (Muzzall and Peebles 1991); Rana pipiens, (Gillilland and Muzzall 1999); Rana sylvatica, (Muzzall and Peebles 1991). Cosmocercoides sp. Wilkie, 1930 Host: Pseudacris c. crucifer, (Muzzall and Peebles 1991). Raillietnema sp. Travassos, 1927 Host: Rana c. melanota, (Muzzall et al. 2001); Rana pipiens, (Gillilland and Muzzall 1999). Aplectana/Cosmocercoides sp. Host: Rana catesbeiana, (Muzzall 1991b); Rana c. melanota, (Muzzall 1991b). Cystidicolidae Skrjabin, 1946 Spinitectus gracilis Ward and Magath, 1917 Host: Rana catesbeiana, (Muzzall 1991b); Rana c. melanota, (Muzzall et al. 2001). Dracunculidae (Stiles, 1907) Leiper, 1912 Dracunculus ophidensis Brackett, 1938 Host: Nerodia s. sipedon, Thamnophis sirtalis, (Brackett 1938). Gnathostomatidae Railliet, 1915 Spiroxys amydae Cobb, 1929 Host: Apalone s. spinifera, (Hedrick 1935). Spiroxys contortus (Rudolphi, 1819) Schneider, 1866 Host: Apalone s. spinifera, Chelydra s. serpentina, Chrysemys picta, Clemmys guttata, Emydoidea blandingi, Graptemys geographica, Sternotherus odoratus, Terrapene c. carolini, (Hedrick 1935); Chrysemys picta, (Esch and Gibbons 1967). Kathlaniidae York and Maplestone, 1926 Falcaustra catesbeianae Walton, 1929 Host: Notophthalmus viridescens, (Muzzall 1991a); Rana catesbeiana, (Muzzall 1991b); Rana c. melanota, (Muzzall 1991b). Falcaustra sp. Lane, 1915 Host: Notophthalmus viridescens, (Muzzall et al. 2003); Rana c. melanota, (Muzzall et al. 2001). Molineidae (Skrjabin and Schulz, 1937) Durette-Desset and Chabaud, 1977 Oswaldocruzia pipiens Walton, 1929 Host: Rana sylvatica, (Muzzall and Peebles 1991). Oswaldocruzia priceae Slimane and Durette Desset 1997 Host: Rana c. melanota, (Muzzall et al. 2001); Rana pipiens, (Gillilland and Muzzall 1999). Oswaldocruzia sp. Travassos, 1917 Host: Rana catesbeiana, Rana c. melanota, Rana pipiens, (Ridgeway 1964). Onchocercidae (Leiper, 1911) Waltonella sp. Schacher, 1974 Host: Rana c. melanota, (Muzzall et al. 2001). Pharyngodonidae Travassos, 1919 Thelandros magnavulvaris (Rankin, 1937) Host: Ambystoma laterale, (Muzzall and Schinderle 1992); Plethodon cinereus, (Muzzall 1990). Rhabdiasidae Railliet, 1915 Rhabdias fuscovenosa (Railliet, 1899) Goodey, 1924 Host: Lampropeltis t. triangulum, Nerodia s. sipedon, Opheodrys vernalis, Thamnophis s. septentrionalis, Thamnophis sirtalis, (Chu 1936a); Nerodia s. sipedon, Thamnophis sirtalis, (Chu 1936b). 15